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Chapter 7 : Porin Regulon of Escherichia coli

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Abstract:

In Escherichia coli, the two porin proteins OmpF and OmpC form pores in the outer membrane that allow for the passive diffusion of small hydrophilic molecules across this hydrophobic barrier. Studies using gene and operon fusions to both ompF and ompC revealed that regulation of porin expression occurs at the transcriptional level. This work, combined with additional genetic analysis, led to the proposal of an early model to explain porin regulation. Importantly, strains merodiploid for envZ473 and either envZ247 or envZ250 exhibit intermediate levels of porin expression that are comparable with that normally seen in low osmolarity. OmpR can activate transcription of both the ompF and ompC genes and can also repress transcription of ompF. To regulate expression of the porin genes, OmpR must interact with regulatory regions of the ompF and ompC promoters in a manner that results in the activation and/or repression of transcription. Much study has been focused on elucidating the following: the regions of DNA to which OmpR binds and the nucleotide sequence of these regions; how OmpR recognizes these regions; and finally, how these OmpR-promoter interactions affect DNA topology, functional interactions with the polymerase, and ultimately transcriptional activation and/or repression. Importantly these conditions mimic those found within the bodies of animals. In external environment surroundings, nutrients are scarce, and the slightly wider OmpF channel enables their more efficient uptake. The smaller, more protective OmpC porin is no longer required in this very dilute environment.

Citation: Pratt L, Silhavy T. 1995. Porin Regulon of Escherichia coli, p 105-127. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch7
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Image of FIGURE 1
FIGURE 1

Domain structure of OmpR and EnvZ. The sensor, EnvZ, is located in the inner membrane with its N-terminal domain in the periplasm and its C-terminal domain in the cytoplasm. It possesses two transmembrane segments extending from 16 to 46 (TM1) and from 163 to 179 (TM2).The N-terminal domain of EnvZ monitors the osmolarity, and this information is transduced across the inner membrane to the C-terminal cytoplasmic domain. The C-terminal portion of EnvZ relays this information to the response regulator, OmpR, via kinase and phosphatase activities. OmpR is a cytoplasmic protein directly responsible for regulating transcription of the ompF and ompC genes. The N-terminal half of OmpR is the phosphorylation domain, containing the acidic pocket and the presumed site of phosphorylation (Asp-55), and the C-teminal portion of OmpR is the DNA binding domain.

Citation: Pratt L, Silhavy T. 1995. Porin Regulon of Escherichia coli, p 105-127. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch7
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Image of FIGURE 2
FIGURE 2

Signaling states of EnvZ. EnvZ must assume different signaling states under varying osmotic conditions. This is accomplished by regulating the ratio of kinase to phosphatase activities such that a phosphatase-dominant state is present in low osmolarity whereas a kinase-dominant state predominates in high osmolarity. The ratio of kinase to phosphatase activities could be regulated by altering either or both enzymatic activities. One possibility is that the ratio is regulated by controlling the relative exposure of the autophosphorylation site, thereby regulating the rate of autophosphorylation (see text for further details).

Citation: Pratt L, Silhavy T. 1995. Porin Regulon of Escherichia coli, p 105-127. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch7
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Image of FIGURE 3
FIGURE 3

Nature of the internal signal. (Top) OmpR assumes different roles under varying osmotic conditions. In low osmolarity (thick line), OmpR functions as a transcriptional activator of ompF, whereas in high osmolarity (thin line), OmpR functions to repress ompF transcription and activate ompC transcription. (Bottom) The distinction between the OmpR in low versus high osmolarity is thought to be a difference in the concentration of OmpR-phosphate. Low concentrations of OmpR favor transcriptional activation of ompF, whereas higher concentrations of OmpR-phosphate repress ompF transcription and activate ompC transcription.

Citation: Pratt L, Silhavy T. 1995. Porin Regulon of Escherichia coli, p 105-127. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch7
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Image of FIGURE 4
FIGURE 4

Porin promoters. OmpR-mediated transcriptional regulation of the porin genes involves extensive regions of promoter DNA. The regions required for positive and negative regulation are indicated above the promoters by (+) and (−), respectively. The regions protected by OmpR in vivo and in vitro are also indicated (see key).

Citation: Pratt L, Silhavy T. 1995. Porin Regulon of Escherichia coli, p 105-127. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch7
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References

/content/book/10.1128/9781555818319.chap7
1. Adler, H. 1966. Chemotaxis in bacteria. Science 153:708716.
2. Aiba, H.,, and T. Mizuno. 1990. Phosphorylation of a bacterial activator protein, OmpR, by a protein kinase, EnvZ, stimulates the transcription of the ompF and ompC genes in Escherichia coli. FEBS Lett. 261:1922.
3. Aiba, H.,, T. Mizuno,, and S. Mizushima. 1989a. Transfer of phosphoryl group between two regulatory proteins involved in osmoregulatory expression of the ompF and ompC genes in Escherichia coli. J. Biol. Chem. 264:85638567.
4. Aiba, H.,, E. Nakasai,, S. Mizushima,, and T. Mizuno. 1989b. Evidence for the physiological importance of the phosphotransfer between the two regulatory components, EnvZ and OmpR, in osmoregulation in Escherichia coli. J. Biol. Chem. 264:1409014094.
5. Aiba, H.,, E. Nakasai,, S. Mizushima,, and T. Mizuno. 1989c. Evidence for the physiological importance of the phosphotransfer between the two regulatory components, EnvZ and OmpR, in osmoregulation in Escherichia coli. J. Biol. Chem. 264:1409014094.
6. Anderson, J.,, S. A. Forst,, K. Zhao,, M. Inouye,, and N. Delihas. 1989. The function of micF RNA. J. Biol. Chem. 264:1796117970.
7. Baumgartner, J. W.,, C. Kim,, R. E. Brissette,, M. Inouye,, C. Park,, and G. L. Hazelbauer. 1994. Transmembrane signalling by a hybrid protein: communication from the domain of chemoreceptor Trg that recognizes sugar-binding proteins to the kinase/phosphatase domain of osmosensor EnvZ. J. Bacteriol. 176:11571163.
8. Chou, J. H.,, J. T. Greenberg,, and B. Demple. 1993. Posttranscriptional repression of Escherichia coli OmpF protein in response to redox stress: positive control of the micF antisense RNA by the soxRS locus. J. Bacteriol. 175:10261031.
9. Comeau, D. E.,, K. Ikenaka,, K. Tsung,, and M. Inouye. 1985. Primary characterization o f the protein products of the Escherichia coli ompB locus: structure and regulation of synthesis of the OmpR and EnvZ proteins J. Bacteriol. 164:578584.
10. Csonka, L. N. 1989. Physiological and genetic responses of bacteria to osmotic stress. Microbiol. Rev. 53:121147.
11. Demple, B. 1991. Regulation of bacterial oxidative stress genes. Annu. Rev. Genet. 25:315337.
12. Fiedler, W.,, and H. Rotering. 1988. Properties of Escherichia coli mutants lacking membrane-derived oligosaccharides. J. Biol. Chem. 263:1468414689.
13. Forst, S.,, D. Comeau,, S. Norioka,, and M. Inouye. 1987. Localization and membrane topology of EnvZ, a protein involved in osmoregulation of OmpF and OmpC in Escherichia coli. J. Biol. Chem. 262:1643316438.
14. Forst, S. J. Delgado, and M. Inouye. 1989. Phosphorylation of OmpR by the osmosensor EnvZ modulates expression of the ompF and ompC genes in Escherichia coli. Proc. Natl. Acad. Sci. USA 86:60526056.
15. Forst, S.,, J. Delgado,, A. Rampersaud,, and M. Inouye. 1990. In vivo phosphorylation of OmpR, the transcription activator of the ompF and ompC genes in Escherichia coli. J. Bacteriol. 172:34733477.
16. Friedman, D. I. 1988. Integration host factor: a protein for all reasons. Cell 55:545554.
17. Garrett, S.,, and T. J. Silhavy. 1987. Isolation of mutations in the α operon of Escherichia coli that suppress the transcriptional defect conferred by a mutation in the porin regulatory gene envZ. J. Bacteriol. 169:13791385.
18. Garrett, S.,, R. Taylor,, and T. J. Silhavy. 1983. Isolation and characterization o f chain-terminating nonsense mutations in a porin regulator gene, envZ. J. Bacteriol. 156:6269.
19. Geiger, O.,, F. D. Russo,, T. J. Silhavy,, and E. P. Kennedy. 1992. Membrane-derived oligosaccharides affect porin osmoregulation only in media of low ionic strength. J. Bacteriol. 174:14101413.
20. Greenberg, J. X.,, P. Monach,, J. H. Chou,, P. D. Josephy,, and B. Demple. 1990. Positive control of a global antioxidant defense regulon activated by superoxide-generating agents in Escherichia coli. Proc. Natl. Acad. Sci. USA 87:61816185.
21. Hall, M. N.,, and T. J. Silhavy. 1979. Transcriptional regulation of Escherichia coli K-12 major outer membrane protein lb.J. Bacteriol. 140:342350.
22. Hall, M. N.,, and T. J. Silhavy. 1981a.The ompB locus and the regulation of the major outer membrane porin proteins of Escherichia coli K-12. J. Mol. Biol. 146:2343.
23. Hall, M. N.,, and T. J. Silhavy. 1981b. Genetic analysis of the ompB locus in Escherichia coli K-12. J. Mol. Biol. 151:115.
24. Hess, J. E.,, R. B. Bourret,, and M. I. Simon. 1988. Histidine phosphorylation and phosphoryl group transfer in bacterial chemotaxis. Nature (London) 336:139143.
25. Huang, K.,, J. L. Schieberl,, and M. M. Igo. 1994. A distant upstream site involved in the negative regulation of the Escherichia coli ompF gene. J. Bacteriol. 176:13091315.
26. Igarashi, K.,, A. Hanamura,, K. Makino,, H. Aiba,, H. Aiba,, T. Mizuno,, A. Nakata,, and A. Ishihama. 1991. Functional map of the a subunit of Escherichia coli RNA polymerase: two modes of transcription activation by positive factors. Proc. Natl. Acad. Sci. USA 88:89588962.
27. Igarashi, K.,, and A. Ishihama. 1991. Bipartite functional map of the E. coli RNA polymerase a subunit: involvement of the C-terminal region in transcription activation by cAMP-CRP. Cell 65: 10151022.
28. Igo, M. M.,, A. J. Ninfa,, and T. J. Silhavy. 1989a. A bacterial environmental sensor that functions as protein kinase and stimulates transcriptional activation. Genes Dev. 3:598605.
29. Igo, M. M.,, A. J. Ninfa,, J. B. Stock,, and T. J. Silhavy. 1989b. Phosphorylation and dephosphorylation of a bacterial transcriptional activator by a transmembrane receptor. Genes Dev. 3:17251734.
30. Igo, M. M.,, and T. J. Silhavy. 1988. EnvZ, a transmembrane environmental sensor of Escherichia coli K-12, is phosphorylated in vitro. J. Bacteriol. 170: 59715973.
31. Inokuchi, K.,, H. Furukawa,, K. Nakamura,, and S. Mizushima. 1984. Characterization by deletion mutagenesis in vitro of the promoter region of ompF, a positively regulated gene of Escherichia coli. J. Mol. Biol. 178:653668.
32. Jin, X.,, and M. Inouye. 1993. Ligand binding to the receptor domain regulates the ratio of kinase to phosphatase activities of the signalling domain of hybrid Escherichia coli transmembrane receptor,Taz1. J. Mol. Biol. 232:484492.
33. Jo, Y.,, F. Nara,, S. Ichihara,, T. Mizuno,, and S. Mizushima. 1986. Purification and characterization of the OmpR protein, a positive regulator involved in osmoregulatory expression of the ompF and ompC genes in Escherichia coli. J. Biol. Chem. 261:1525215256.
34. Keeney, L.,, and T. J. Silhavy. Unpublished data.
35. Kofoid, E. C.,, and J. S. Parkinson. 1988. Transmitter and receiver modules in bacterial signaling proteins. Proc. Natl. Acad. Sci. USA 85:49814985.
36. Kondo, H.,, T. Miyaji,, M. Suzuki,, S. Tate,, T. Mizuno,, Y. Nishimura,, and I. Tanaka. 1994. Crystallization and X-ray studies of the DNAbinding domain of OmpR protein, a positive regulator involved in activation of osmoregulatory genes in Escherichia coli. J. Mol. Biol. 235:780782.
37. Lange, R.,, and R. Hengge-Aronis. 1991. Identification of a central regulator of stationary phase gene expression in E. coli. Mol. Microbiol. 5:4959.
38. Liljestrom, P. 1986. The EnvZ protein of Salmonella typhimurium LT-2 and Escherichia coli K-12 is located in the cytoplasmic membrane. FEMS Microbiol. Lett. 36:145150.
39. Maeda, S.,, and T. Mizuno. 1988. Activation of the ompC gene by the OmpR protein in Escherichia coli. J. Biol. Chem. 263:1462914633.
40. Maeda, S.,, and T. Mizuno. 1990. Evidence for multiple OmpR-binding sites in the upstream activation sequence of the ompC promoter in Escherichia coli: a single OmpR-binding site is capable of activating the promoter. J. Bacteriol. 172:501503.
41. Matsuyama, S.,, and S. Mizushima. 1985. Construction and characterization of a deletion mutant lacking micF, a proposed regulatory gene for OmpF synthesis in Escherichia coli. J. Bacteriol. 162:11961202.
42. Matsuyama, S.,, and S. Mizushima. 1987. Novel rpoA mutation that interferes with the function of OmpR and EnvZ, positive regulators of the ompF and ompC genes that code for outer-membrane proteins in Escherichia coli K12. J. Mol. Biol. 195:847853.
43. McCann, M. P.,, J. P. Kidwell,, and A. Matin. 1991. The putative O" factor KatF has a central role in development of starvation-mediated general resistance in Escherichia coli. J. Bacteriol. 173:41884194.
44. Mizuno, T. 1987. Static bend of DNA helix at the activator recognition site of the ompF promoter in Escherichia coli. Gene 54:5764.
45. Mizuno, X.,, M. Chou,, and M. Inouye. 1983. A comparative study on the genes for three porins of the Escherichia coli outer membrane. J. Biol. Chem. 258:69326940.
46. Mizuno, X.,, M. Chou,, and M. Inouye. 1984. A unique mechanism regulating gene expression:translational inhibition by a complementary RNA transcript (micRNA). Proc. Natl. Acad. Sci. USA 81:19661970.
47. Mizuno, T.,, M. Kato,, Y. Jo,, and S. Mizushima. 1988. Interaction of OmpR, a positive regulator, with the osmoregulated ompC and ompF genes of Escherichia coli. J. Biol. Chem. 263:10081012.
48. Mizuno, T.,, and S. Mizushima. 1986. Characterization by deletion and localized mutagenesis in vitro of the promoter region of the Escherichia coli ompC gene and importance of the upstream DNA domain in positive regulation by the OmpR protein. J. Bacteriol. 168:8695.
49. Nakashima, K.,, K. Kanamuru,, H. Aiba,, and T. Mizuno. 1991. Signal transduction and osmoregulation in Escherichia coli. J. Biol. Chem. 266:1077510780.
50. Nara, E.,, S. Matsuyama,, T. Mizuno,, and S. Mizushima. 1986. Molecular analysis of mutant ompR genes exhibiting different phenotypes as to osmoregulation of the ompF and ompC genes of Escherichia coli. Mol. Gen. Genet. 202:194199.
51. Nikaido, H.,, and M. Vaara,. 1987. Outer membrane, p. 722. In F. C. Neidhardt (ed.), Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology. American Society for Microbiology, Washington, DC..
52. Ninfa, A. J.,, and B. Magasanik. 1986. Covalent modification of the glnG product, NR|, by the glnALG product, NRn, regulates the transcription of the glnALG operon in Escherichia coli. Proc. Natl. Acad. Sci. USA 83:59095913.
53. Ninfa, G. E.,, A. Stock,, S. Mowbray,, and J. Stock. 1991. Reconstitution of the bacterial chemotaxis signal transduction system from purified components. J. Biol. Chem. 266:97649770.
54. Norioka, S.,, G. Ramakrishnan,, K. Dcenaka,, and M. Inouye. 1986. Interaction of a transcriptional activator, OmpR, with reciprocally osmoregulated genes, ompF and ompC, of Escherichia coli. J. Biol. Chem. 261:1711317119.
55. Ostrow, K. S.,, T. J. Silhavy,, and S. Garrett. 1986. as-Acting sites required for osmoregulation of ompF expression in Escherichia coli K-12. J. Bacteriol. 168:11651171.
56. Parkinson, J. S. 1993. Signal transduction schemes in bacteria. Cell 73:857871.
57. Pratt, L.,, and T. J. Silhavy. Unpublished data.
58. Pratt, L. P.,, and T. J. Silhavy. 1994. OmpR mutants specifically defective for transcriptional activation.J. Mol. Biol. 243:579594.
59. Ramani, N.,, M. Hedeshian,, and M. Freundlich. 1994. micF antisense RNA has a major role in osmoregulation of OmpF in Escherichia coli. J. Bacteriol. 76:50055010.
60. Ramani, N.,, L. Huang,, and M. Freundlich. 1992. In vitro interactions of integration host factor with the ompF promoter-regulatory region of Escherichia coli. Mol. Gen. Genet. 231:248255.
61. Rampersaud, A.,, S. L. Harlocker,, and M. Inouye. 1994. The OmpR protein of Escherichia coli binds to sites in the ompF promoter region in a hierarchical manner determined by its degree of phosphorylation. J. Biol. Chem. 269:1255912566.
62. Roberts, D. L.,, D. W. Bennet,, and S. A. Forst. 1994. Identification of the site of phosphorylation on the osmosensor, EnvZ, of Escherichia coli. J. Biol. Chem. 269:87288733.
63. Russo, F. D. 1992. Ph.D. thesis. Princeton University, Princeton, N J.
64. Russo, E.,, and T. J. Silhavy. 1991. EnvZ controls the concentration of phosphorylated OmpR to mediate osmoregulation of the porin genes. J. Mol. Biol. 222:567580.
65. Russo, E.,, and T. J. Silhavy. 1992. Alpha: the Cinderella subunit of RNA polymerase. J. Biol. Chem. 267:1451514518.
66. Russo, E.,, J. M. Slauch,, and T. J. Silhavy. 1993. Mutations that affect separate functions of OmpR the phosphorylated regulator of porin transcription in Escherichia coli. J. Mol. Biol. 231:261273.
67. Sarma, V.,, and P. Reeves. 1977. Genetic locus (ompB) affecting a major outer-membrane protein in Escherichia coli K 12. J Bacteriol. 132:2327.
68. Sato, T.,, and T. Tura. 1979. Chromosomal location and expression of the structural gene for major outer membrane protein la of Escherichia coli K-12 and o f the homologous gene of Salmonella typhimurium. J. Bacteriol. 139:468477.
69. Sharif, R. T.,, and M. M. Igo. 1993. Mutations in the alpha subunit of RNA polymerase that affect the regulation of porin gene transcription in Escherichia coli K-12. J. Bacteriol. 175:54605468.
70. Slauch, J. M.,, and T. J. Silhavy. 1989. Genetic analysis of the switch that controls porin gene expression in Escherichia coli. J. Mol. Biol. 210:281292.
71. Slauch, J. M.,, and T. J. Silhavy. 1991. cis- Acting ompF mutations that result in OmpR-dependent constitutive expression. J. Bacteriol. 173:40394048.
72. Slauch, J. M.,, F. D. Russo,, and T. J. Silhavy. 1991. Suppressor mutations in rpoA suggest that OmpR controls transcription by direct interaction with the a subunit of RNA polymerase. J. Bacteriol. 173:75017510.
73. Stock, A. M.,, J. M. Mottonen,, J. B. Stock,, and C. E. Schutt. 1989. Three-dimensional structure of CheY, the response regulator o f bacterial chemotaxis. Nature (London) 337:745749.
74. Stock, J. B.,, B. Rauch,, and S. Roseman. 1977. Periplasmic space in Salmonella typhimurium and Escherichia coli. J. Biol. Chem. 252:78507861.
75. Stock, J. B.,, A. M. Stock,, and J. M. Mottonen. 1990. Signal transduction in bacteria. Nature (London) 344:395400.
76. Takayanagi, K.,, S. Maeda,, and T. Mizuno. 1991. Expression of micF involved in porin synthesis in Escherichia coli: two distinct rii-acting elements respectively regulate micF expression positively and negatively. FEMS Microbiol. Lett. 83:3944.
77. Tate, S.,, M. Kato,, Y. Nishimura,, Y. Arata,, and T. Mizuno. 1988. Location of DNA-binding segment of a positive regulator, OmpR, involved in activation of the ompF and ompC genes of Escherichia coli. FEBS Lett. 242:2730.
78. Taylor, R. T.,, S. Garrett,, E. Sodergren,, and T. J. Silhavy. 1985. Mutations that define the promoter of ompF, a gene specifying a major outer membrane porin protein J. Bacteriol. 162:10541060.
79. Tokishita, S.,, A. Kojima,, H. Aiba,, and T. Mizuno. 1991. Transmembrane signal transduction and osmoregulation in Escherichia coli. J. Biol. Chem. 266:67806785.
80. Tokishita, S.,, A. Kojima,, and T. Mizuno. 1992. Transmembrane signal transduction and osmoregulation in Escherichia coli: functional importance of the transmembrane regions of membrane-located protein kinase, EnvZ. J. Biochem. 111:707713.
81. Tsui, P.,, V. Helu,, and M. Freundlich. 1988. Altered osmoregulation of ompF in integration host factor mutants of Escherichia coli. J. Bacteriol. 170:49504953.
82. Tsung, K.,, R. E. Brissette,, and M. Inouye. 1989. Identification of the DNA-binding domain of the OmpR protein required for transcriptional activation of the ompF and ompC genes of Escherichia coli by in vivo DNA footprinting. J. Biol. Chem. 264:1010410109.
83. Utsumi, R.,, R. E. Brissette,, A. Rampersaud,, S. A. Forst,, K. Oosawa,, and M. Inouye. 1989. Activation of bacterial porin gene expression by a chimeric signal transducer in response to aspartate. Science 245:12461249.
84. Van Alphen, W.,, and B. Lugtenberg. 1977. Influence of osmolarity of the growth medium on the outer membrane protein pattern of Escherichia coli. J. Bacteriol. 131:623630.
85. Verhoef, C.,, P. J. de Graaff,, and E. J. J. Lugtenberg. 1977. Mapping of a gene for a major outer membrane protein of Escherichia coli K12 with the aid of a newly isolated bacteriophage. Mol. Gen. Genet. 150:103105.
86. Volz, K.,, and P. Matsumura. 1991. Crystal structure of Escherichia coli CheY refined at 1.7-A resolution. J. Biol. Chem. 266:1551115519.
87. Waukau, J.,, and S. Forst. 1992. Molecular analysis of the signaling pathway between EnvZ and OmpR in Escherichia coli. J. Bacteriol. 174:15221527.
88. Wurtzel, E. T.,, M. Y. Chou,, and M. Inouye. 1982. Osmoregulation of gene expression I. DNA sequence of the ompR gene of the ompB operon of Escherichia coli and characterization of its gene product. J. Biol. Chem. 257:1368513691.
89. Wylie, D.,, A. Stock,, C. Wong,, and J. Stock. 1988. Sensory transduction in bacterial chemotaxis involves phosphotransfer between Che proteins. Biochem. Biophys. Res. Commun. 151:891896.
90. Yang, Y.,, and M. Inouye. 1991. Intermolecular complementation between two defective mutant signaltransduction receptors o f Escherichia coli. Proc. Natl. Acad. Sci. USA 88:1105711061.
91. Yang, Y.,, and M. Inouye. 1993. Requirement of both kinase and phosphatase activities of an Escherichia coli receptor (Tazl) for ligand-dependent signal transduction J. Mol. Biol. 231:335342.

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